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Multilocus Sequence Analysis of Root Nodule Bacteria Associated with Lupinus Spp

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Multilocus Sequence Analysis of Root Nodule Bacteria Associated with Lupinus Spp Advances in Microbiology, 2017, 7, 790-812 http://www.scirp.org/journal/aim ISSN Online: 2165-3410 ISSN Print: 2165-3402 Multilocus Sequence Analysis of Root Nodule Bacteria Associated with Lupinus spp. and Glycine max Dilshan H. Beligala, Helen J. Michaels, Michael Devries, Vipaporn Phuntumart* Department of Biological Sciences, Bowling Green State University, Bowling Green, OH, USA How to cite this paper: Beligala, D.H., Abstract Michaels, H.J., Devries, M. and Phuntu- mart, V. (2017) Multilocus Sequence Anal- Lupinus is known to form endophytic associations with both nodulating and ysis of Root Nodule Bacteria Associated non-nodulating bacteria. In this study, multilocus sequence analysis (MLSA) with Lupinus spp. and Glycine max. Ad- was used to analyze phylogenetic relationships among root nodule bacteria vances in Microbiology, 7, 790-812. associated with Lupinus and soybean. Out of 17bacterial strains analyzed, 13 https://doi.org/10.4236/aim.2017.711063 strains isolated from root nodules of Lupinus spp. were obtained from the Na- Received: October 27, 2017 tional Rhizobium Germplasm Resource Collection, USDA. Additionally, two Accepted: November 27, 2017 strains of root-nodule bacteria isolated each from native Lupinus and domes- Published: November 30, 2017 tic soybean were examined. Sequences of the 16S rRNA gene and three Copyright © 2017 by authors and housekeeping genes (atpD, dnaK and glnII) were used. All the reference genes Scientific Research Publishing Inc. were retrieved from the existing complete genome sequences only. The clus- This work is licensed under the Creative tering of 12 of the strains was consistent among single and concatenated gene Commons Attribution International trees, but not USDA strains 3044, 3048, 3504, 3715, and 3060. According to License (CC BY 4.0). the concatenated phylogeny, we suggest that USDA 3040, 3042, 3044, 3048, http://creativecommons.org/licenses/by/4.0/ Open Access 3051, 3060, 3504, 3709 and 3715 are Bradyrhizobium, USDA 3063 and 3717 are Mesorhizobium, USDA 3043 is Burkholderia and USDA 3057a is Micro- virga. The two strains isolated from native lupines in this study are Burkhol- deria and Rhizobium, whereas the two from domestic soybean are Bradyrhi- zobium. This study emphasizes the robustness of MLSA, the diversity of bac- terial species that are capable of nodulating lupine and the substantial capabil- ity of Burkholderia spp. to colonize lupine root nodules. Keywords Multilocus Sequence Analysis, Nodule Bacteria, Phylogeny, Lupinus, Burkholderia 1. Introduction The plant family Fabaceae or Leguminosae is considered the third largest family DOI: 10.4236/aim.2017.711063 Nov. 30, 2017 790 Advances in Microbiology D. H. Beligala et al. of flowering plants and is well known for its important ecological function in fixing atmospheric nitrogen. It is comprised of three subfamilies Caesalpinioi- deae, Mimosoideae and Faboideae. Within the Genisteae tribe of the legume subfamily Faboideae, the genus Lupinus or lupine encompasses more than 280 species of annual herbs and perennial herbaceous and woody shrubs distributed mainly in South and Western North America, the Andes, the Mediterranean re- gions and Africa [1]. Because of this ability to establish symbiotic associations with bacteria that can fix atmospheric nitrogen in root nodules, members of the genus Lupinus thrive in nutrient poor soils. The rhizobial requirement of Lupi- nus has been thought to be somewhat specific, with literature indicating that lu- pines are mainly nodulated by soil bacteria classified in the genus Bradyrhizo- bium, although some other rhizobial and endophytic genera nodulating lupines have been identified as Mesorhizobium, Rhizobium, Microvirga, Paenibacillus, Micromonospora, Bosea, Ochrobactrum and Cohnella [2]-[14]. In addition, members of the genus Burkholderia (in class Betaproteobacteria) are known as endophytic bacteria in lupine [15] and considered the major inhabitants of white lupine cluster roots [16]. Previously, the 16S rRNA gene sequence was most commonly used in bacteri- al phylogenetic studies because of its slow mutation rate due to functional im- portance. The 16S rRNA sequence is genus specific and hence provides genus identification in more than 90% of the cases [17] [18]. However, there are some drawbacks associated with the use of 16S rRNA gene sequences such as the presence of mosaicism in the 16S rRNA gene due to horizontal gene transfer and recombination events, the presence of multiple copies of the rRNA operon and the low resolution of closely related species [2]. Multilocus sequence analysis (MLSA), which combines analysis of several conserved housekeeping genes [19], provides improved discriminatory power over the use of single locus sequence and thus, it has been increasingly used in phylogenetic analysis of prokaryotes [20] [21] [22] [23] [24]. For the genus Bradyrhizobium, a database for the tax- onomic and phylogenetic identification using MLSA is available online at http://mlsa.cnpso.embrapa.br [25]. In this study, we analyzed 17 bacterial strains, of which 13 had been isolated from root nodules of Lupinus spp. from different geographic locations at various times (kindly provided by the National Rhizobium Germplasm Resource Collec- tion, USDA). Additionally, two samples each from root nodules of native Sundi- al lupine (Lupinus perennis) and domestic soybean (Glycine max) were isolated from plants grown in OH, USA. We applied MLSA to assess the genetic diversity and phylogenetic relationships of these strains using sequence analysis of the 16S rRNA gene and three conserved housekeeping genes (atpD, dnaK and glnII). These housekeeping genes have been widely used in phylogenetic analyses due to their sequence and functional conservation. Additionally, there are a large num- ber of sequences available in the databases. The atpD gene encodes the beta subunit of ATP synthase that produces ATP from ADP in the presence of a pro- DOI: 10.4236/aim.2017.711063 791 Advances in Microbiology D. H. Beligala et al. ton gradient across the membrane [26] [27]. The dnaK gene encodes the DnaK protein, which functions as a molecular chaperone responsible for various cellu- lar processes, such as folding of nascent polypeptides, assembly and disassembly of protein complexes, protein degradation and membrane translocation of se- creted proteins [2] [4]. The glnII gene encodes glutamine synthetase II which catalyzes the condensation of glutamate and ammonia to form glutamine [21] [28] [29] [30]. Our study is distinct because all the reference gene sequences were extracted from the existing complete genomes that are available via the In- tegrated Microbial Genomes database [31]. The phylogenetic tree based on the concatenated sequences comparing the 17 strains with 30 reference strains sug- gests that MLSA provides improved taxonomic relationships of these bacterial strains. 2. Materials and Methods 2.1. Bacterial Strains A total of 17 strains from at least ten geographic locations were examined in this study (Table 1), including USA, Yugoslavia and Brazil; 13 strains were obtained from the National Rhizobium Germplasm Resource Collection, USDA. Two strains each were isolated from nodules of locally grown (Bowling Green, OH, Table 1. Bacterial strains. Strain Host Origin, collected time Suggested identification USDA 3040 L. albus FL, USA, 1940 Bradyrhizobium USDA 3042 L. albus Yugoslavia, 1955 Bradyrhizobium USDA 3051 L. angustifolius GA, USA, 1946 Bradyrhizobium USDA 3063 L. densiflorus CA, USA, 1962 bMesorhizobium USDA 3044 L. luteus FL, USA, 1946 Bradyrhizobium USDA 3048 L. luteus Brazil, 1959 Bradyrhizobium USDA 3504 L. mutabilis Unknown Bradyrhizobium USDA 3715 L. nanus CA, USA, 1922 Bradyrhizobium USDA 3043 L. perennis MD, USA, 1941 bBurkholderia USDA 3709 L. polyphyllus aNitragin, unknown location, 1945 Bradyrhizobium USDA 3057a L. subcarnosus aNitragin, FL, USA, 1946 bMicrovirga USDA 3717 L. succulentus CA, USA, 1973 Mesorhizobium USDA 3060 L. spp aNitragin, unknown Bradyrhizobium Kitty Todd Nature Preserve, Swanton, L_OO L. perennis Burkholderia OH, 2014 (this study) L_3D52 L. perennis Bowling Green, OH, 2014 (this study) Rhizobium SB_J Glycine max Bowling Green, OH, 2014 (this study) Bradyrhizobium SB_5 Glycine max Bowling Green, OH, 2014 (this study) Bradyrhizobium aSeed company; bPreviously reported as Bradyrhizobium. DOI: 10.4236/aim.2017.711063 792 Advances in Microbiology D. H. Beligala et al. USA) Lupinus perennis and Glycine max. The USDA strains had been collected between 1922-73, while the nodules from native lupine and domestic soybean were collected in October 2014 and July 2014, respectively. To isolate bacteria from root nodules, the collected nodules were surface sterilized by the method described by Deng [32], with some modifications. Briefly, the nodules were washed with sterile distilled water three times for 30 sec, soaked in 10% Clorox for 30 sec, followed by rinsing with distilled water for 30 sec, then with 70% ethanol for 10 min, after which they were rinsed three times with sterile distilled water. A sterile glass rod was used to crush root nodules from each sample fol- lowed by streaking the suspension onto modified arabinose gluconate medium [33] with a sterile inoculating loop. The cultures were incubated at 30˚C. Initial verification was conducted by colony morphology and Gram stain. All the strains were maintained at 4˚C for temporary storage and in 20% glycerol at −80˚C for long term storage. 2.2. DNA Extraction, PCR and Sequencing Total genomic
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